UbiN, a novel Rhodobacter capsulatus decarboxylative hydroxylase involved in aerobic ubiquinone biosynthesis
Ubiquinone (UQ) is a lipophilic electron carrier that functions in the respiratory and photosynthetic electron transfer chains of proteobacteria and eukaryotes. Bacterial UQ biosynthesis is well studied in the gammaproteobacterium Escherichia coli, in which most bacterial UQ‐biosynthetic enzymes hav...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Wiley
2023-11-01
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| Series: | FEBS Open Bio |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/2211-5463.13707 |
| _version_ | 1797635905977057280 |
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| author | Haruka Nagatani Yoshiyuki Mae Miharu Konishi Motomichi Matsuzaki Kiyoshi Kita Fevzi Daldal Kimitoshi Sakamoto |
| author_facet | Haruka Nagatani Yoshiyuki Mae Miharu Konishi Motomichi Matsuzaki Kiyoshi Kita Fevzi Daldal Kimitoshi Sakamoto |
| author_sort | Haruka Nagatani |
| collection | DOAJ |
| description | Ubiquinone (UQ) is a lipophilic electron carrier that functions in the respiratory and photosynthetic electron transfer chains of proteobacteria and eukaryotes. Bacterial UQ biosynthesis is well studied in the gammaproteobacterium Escherichia coli, in which most bacterial UQ‐biosynthetic enzymes have been identified. However, these enzymes are not always conserved among UQ‐containing bacteria. In particular, the alphaproteobacterial UQ biosynthesis pathways contain many uncharacterized steps with unknown features. In this work, we identified in the alphaproteobacterium Rhodobacter capsulatus a new decarboxylative hydroxylase and named it UbiN. Remarkably, the UbiN sequence is more similar to a salicylate hydroxylase than the conventional flavin‐containing UQ‐biosynthetic monooxygenases. Under aerobic conditions, R. capsulatus ΔubiN mutant cells accumulate 3‐decaprenylphenol, which is a UQ‐biosynthetic intermediate. In addition, 3‐decaprenyl‐4‐hydroxybenzoic acid, which is the substrate of UQ‐biosynthetic decarboxylase UbiD, also accumulates in ΔubiN cells under aerobic conditions. Considering that the R. capsulatus ΔubiD‐X double mutant strain (UbiX produces a prenylated FMN required for UbiD) grows as a wild‐type strain under aerobic conditions, these results indicate that UbiN catalyzes the aerobic decarboxylative hydroxylation of 3‐decaprenyl‐4‐hydroxybenzoic acid. This is the first example of the involvement of decarboxylative hydroxylation in ubiquinone biosynthesis. This finding suggests that the C1 hydroxylation reaction is, at least in R. capsulatus, the first step among the three hydroxylation steps involved in UQ biosynthesis. Although the C5 hydroxylation reaction is often considered to be the first hydroxylation step in bacterial UQ biosynthesis, it appears that the R. capsulatus pathway is more similar to that found in mammalians. |
| first_indexed | 2024-03-11T12:27:36Z |
| format | Article |
| id | doaj.art-7cbf11671e7e443f9b7b529be6fe80f1 |
| institution | Directory Open Access Journal |
| issn | 2211-5463 |
| language | English |
| last_indexed | 2024-03-11T12:27:36Z |
| publishDate | 2023-11-01 |
| publisher | Wiley |
| record_format | Article |
| series | FEBS Open Bio |
| spelling | doaj.art-7cbf11671e7e443f9b7b529be6fe80f12023-11-06T07:27:07ZengWileyFEBS Open Bio2211-54632023-11-0113112081209310.1002/2211-5463.13707UbiN, a novel Rhodobacter capsulatus decarboxylative hydroxylase involved in aerobic ubiquinone biosynthesisHaruka Nagatani0Yoshiyuki Mae1Miharu Konishi2Motomichi Matsuzaki3Kiyoshi Kita4Fevzi Daldal5Kimitoshi Sakamoto6United Graduate School of Agricultural Sciences Iwate University Morioka JapanFaculty of Agriculture and Life Science Hirosaki University JapanFaculty of Agriculture and Life Science Hirosaki University JapanRIKEN Center for Advanced Intelligence Project Tokyo JapanSchool of Tropical Medicine and Global Health Nagasaki University JapanDepartment of Biology University of Pennsylvania Philadelphia PA USAUnited Graduate School of Agricultural Sciences Iwate University Morioka JapanUbiquinone (UQ) is a lipophilic electron carrier that functions in the respiratory and photosynthetic electron transfer chains of proteobacteria and eukaryotes. Bacterial UQ biosynthesis is well studied in the gammaproteobacterium Escherichia coli, in which most bacterial UQ‐biosynthetic enzymes have been identified. However, these enzymes are not always conserved among UQ‐containing bacteria. In particular, the alphaproteobacterial UQ biosynthesis pathways contain many uncharacterized steps with unknown features. In this work, we identified in the alphaproteobacterium Rhodobacter capsulatus a new decarboxylative hydroxylase and named it UbiN. Remarkably, the UbiN sequence is more similar to a salicylate hydroxylase than the conventional flavin‐containing UQ‐biosynthetic monooxygenases. Under aerobic conditions, R. capsulatus ΔubiN mutant cells accumulate 3‐decaprenylphenol, which is a UQ‐biosynthetic intermediate. In addition, 3‐decaprenyl‐4‐hydroxybenzoic acid, which is the substrate of UQ‐biosynthetic decarboxylase UbiD, also accumulates in ΔubiN cells under aerobic conditions. Considering that the R. capsulatus ΔubiD‐X double mutant strain (UbiX produces a prenylated FMN required for UbiD) grows as a wild‐type strain under aerobic conditions, these results indicate that UbiN catalyzes the aerobic decarboxylative hydroxylation of 3‐decaprenyl‐4‐hydroxybenzoic acid. This is the first example of the involvement of decarboxylative hydroxylation in ubiquinone biosynthesis. This finding suggests that the C1 hydroxylation reaction is, at least in R. capsulatus, the first step among the three hydroxylation steps involved in UQ biosynthesis. Although the C5 hydroxylation reaction is often considered to be the first hydroxylation step in bacterial UQ biosynthesis, it appears that the R. capsulatus pathway is more similar to that found in mammalians.https://doi.org/10.1002/2211-5463.13707coenzyme Qdecarboxylative hydrolaseflavin monooxygenaseRhodobacter capsulatusubiquinone biosynthesis |
| spellingShingle | Haruka Nagatani Yoshiyuki Mae Miharu Konishi Motomichi Matsuzaki Kiyoshi Kita Fevzi Daldal Kimitoshi Sakamoto UbiN, a novel Rhodobacter capsulatus decarboxylative hydroxylase involved in aerobic ubiquinone biosynthesis FEBS Open Bio coenzyme Q decarboxylative hydrolase flavin monooxygenase Rhodobacter capsulatus ubiquinone biosynthesis |
| title | UbiN, a novel Rhodobacter capsulatus decarboxylative hydroxylase involved in aerobic ubiquinone biosynthesis |
| title_full | UbiN, a novel Rhodobacter capsulatus decarboxylative hydroxylase involved in aerobic ubiquinone biosynthesis |
| title_fullStr | UbiN, a novel Rhodobacter capsulatus decarboxylative hydroxylase involved in aerobic ubiquinone biosynthesis |
| title_full_unstemmed | UbiN, a novel Rhodobacter capsulatus decarboxylative hydroxylase involved in aerobic ubiquinone biosynthesis |
| title_short | UbiN, a novel Rhodobacter capsulatus decarboxylative hydroxylase involved in aerobic ubiquinone biosynthesis |
| title_sort | ubin a novel rhodobacter capsulatus decarboxylative hydroxylase involved in aerobic ubiquinone biosynthesis |
| topic | coenzyme Q decarboxylative hydrolase flavin monooxygenase Rhodobacter capsulatus ubiquinone biosynthesis |
| url | https://doi.org/10.1002/2211-5463.13707 |
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